Changes in the prevalence of avian disease and mosquito vectors at Hakalau Forest National Wildlife Refuge: a 14-year perspective and assessment of future risk

Abstract

Throughout the main Hawaiian Islands, introduced mosquito-borne disease has had, and continues to have, a profound impact on the distributions and abundance of native Hawaiian forest birds. Populations of remaining native forest birds are largely restricted to high elevation forests where mean temperatures are marginal for vector and parasite development and limited availability of larval mosquito habitat constrains mosquito populations and disease transmission. Hakalau Forest National Wildlife Refuge (HFNWR) was established for the preservation of endemic avifauna in 1985. Since its creation, native bird communities there have remained intact and most species populations are stable or increasing. However, avian malaria had been detected at HFNWR in the past and, in light of documented climate change, new concerns have been raised regarding the long-term fate of the refuge’s forest birds. To examine the possible changes in avian malaria transmission at HFNWR we sampled forest birds for blood parasites, trapped adult mosquitoes and surveyed larval mosquito habitat at three sites during 2012 and compared our results with similar data collected between 1998 and 1999. We tested blood samples by polymerase chain reaction (PCR), immunoblotting, and microscopy to determine prevalence of acute and chronic infection and used attractive gravid traps to sample the vector mosquito Culex quinquefasciatus. Our study documented spatial trends and temporal changes in the prevalence of avian malaria, mosquito presence, larval mosquito habitat and feral pig activity at HFNWR. We found evidence of local transmission in high elevation forests, a general pattern of increasing prevalence at lower elevations and along a South to North gradient and a two-fold decrease in the prevalence of avian malaria in the intervening 14 years. Despite considerable effort, we were unable to detect larval C. quinquefasciatus and captured only one adult indicating that the vector of avian malaria has a very limited presence at HFNWR. We did, however, document the establishment of another invasive mosquito, Aedes japonicus japonicus , and its occurrence in tree fern cavities and rock pools as larval habitat in the lower forests of HFNWR. We suggest that interspecific competition by A. j. japonicus and predation by a suite of native predators may provide biotic resistance to the establishment of permanent C. quinquefasciatus populations. While current predictions of climate change in the Hawaiian Islands include a gradual warming and enhanced transmission by mid-century, the current cooling trend recorded at high elevation HFNWR illustrates the importance of monitoring to document fine scale temporal and site specific changes in prevalence. Long term changes in precipitation may have a more profound effect on local transmission of malaria than temperature and we may have already seen some potential impacts of an extended drought at HFNWR with a decrease in feral pig activity and pig associated larval mosquito habitat and increases in stream-associated larval mosquito habitat.